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Ancestral role of Pax2/5/8 in molluscan brain and multimodal sensory system development.

Wollesen T, Rodríguez Monje SV, Todt C, Degnan BM, Wanninger A - BMC Evol. Biol. (2015)

Bottom Line: Our results, along with those on Otx- and Hox-gene expression, demonstrate that the cephalopod condition is similar to that in mouse and fruit fly, with Otx being expressed in the anterior-most brain region (except for the vertical lobe) and a Pax2/5/8 expression domain separating the Otx-domain from a Hox-gene expressing posterior brain region.Thus, Pax2/5/8 appears to have been recruited independently into regionalization of non-homologous complex brains of organisms as different as squid, fruit fly, and mouse.In mollusks, Pax2/5/8 is only expressed in derivatives of the ectoderm and hence an ancestral role in molluscan ectoderm differentiation is inferred.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Zoology, Faculty of Sciences, University of Vienna, 1090, Vienna, Austria. tim.wollesen@univie.ac.at.

ABSTRACT

Background: Mollusks represent the largest lophotrochozoan phylum and exhibit highly diverse body plans. Previous studies have demonstrated that transcription factors such as Pax genes play important roles during their development. Accordingly, in ecdysozoan and vertebrate model organisms, orthologs of Pax2/5/8 are among others involved in the formation of the midbrain/hindbrain boundary, the auditory/geosensory organ systems, and the excretory system.

Methods: Pax2/5/8 expression was investigated by in situ hybridization during the development of representatives of the two major molluscan subclades, Aculifera and Conchifera.

Results: Compared to the investigated polyplacophoran and bivalve species that lack larval statocysts as geosensory organs and elaborate central nervous systems (CNS), cephalopods possess highly centralized brains and statocysts. Pax2/5/8 is expressed in regions where sensory cells develop subsequently during ontogenesis. Expression domains include esthetes and the ampullary system in polyplacophorans as well as the eyes of cephalopods. No Pax2/5/8 expression was observed in the less centralized CNS of bivalve, polyplacophoran, and gastropod embryos, thus arguing for a loss of Pax2/5/8 involvement in CNS development in these lineages. In contrast, Pax2/5/8 is expressed among others in brain lobes along the trajectory of the esophagus that divides the cephalopod brain.

Conclusions: Our results, along with those on Otx- and Hox-gene expression, demonstrate that the cephalopod condition is similar to that in mouse and fruit fly, with Otx being expressed in the anterior-most brain region (except for the vertical lobe) and a Pax2/5/8 expression domain separating the Otx-domain from a Hox-gene expressing posterior brain region. Thus, Pax2/5/8 appears to have been recruited independently into regionalization of non-homologous complex brains of organisms as different as squid, fruit fly, and mouse. In addition, Pax2/5/8 is expressed in multimodal sensory systems in mollusks such as the esthetes and the ampullary system of polyplacophorans as well as the eyes of cephalopods. Pax2/5/8-expressing cells are present in regions where the future sensory cells such as the polyplacophoran esthetes are situated and hence Pax2/5/8 expression probably predates sensory cell development during ontogeny. In mollusks, Pax2/5/8 is only expressed in derivatives of the ectoderm and hence an ancestral role in molluscan ectoderm differentiation is inferred.

No MeSH data available.


Related in: MedlinePlus

Sketch drawings of Pax2/5/8 expression in Acanthochitona crinita, Nucula tumidula, and Idiosepius notoides. Dorsal (d)–ventral (v), apical (a)-abapical (aa), and anterior (ant)-posterior (p) axes indicate the orientation. Mouth is marked by asterisk in all panels. Pax2/5/8-expressing cell groups are indicated by red numbers in early trochophore larvae of Acanthochitona crinita (first row). Additional Pax2/5/8-expressing cells are located in the hyposphere of further developed larvae (second row). A pericalymma larva (third row) and a settled individual (fourth row) of Nucula tumidula express Pax2/5/8 in the mantle. Note that Pax2/5/8 is not expressed in the test cells (tc) that constitute the outermost cell layer. A stage 19 individual (fifth row) and a stage 24–25 individual (sixth row) of Idiosepius notoides express Pax2/5/8 in various domains. Red dashed line indicates trajectory of esophagus and internal yolk. Abbreviations: an, anus; at, apical tuft, ey, eye; f, foot; fn, funnel; g, gill; ib, interbasal lobe; m, mantle; ms, middle subesophageal mass; s, shell; sc, statocyst; sg, shell gland; se, supraesophageal mass; stm, stomach; ps, posterior subesophageal mass; pt, prototroch; y, yolk. Scale bars: 50 μm (except both last scale bars for I. notoides with 150 μm)
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Fig5: Sketch drawings of Pax2/5/8 expression in Acanthochitona crinita, Nucula tumidula, and Idiosepius notoides. Dorsal (d)–ventral (v), apical (a)-abapical (aa), and anterior (ant)-posterior (p) axes indicate the orientation. Mouth is marked by asterisk in all panels. Pax2/5/8-expressing cell groups are indicated by red numbers in early trochophore larvae of Acanthochitona crinita (first row). Additional Pax2/5/8-expressing cells are located in the hyposphere of further developed larvae (second row). A pericalymma larva (third row) and a settled individual (fourth row) of Nucula tumidula express Pax2/5/8 in the mantle. Note that Pax2/5/8 is not expressed in the test cells (tc) that constitute the outermost cell layer. A stage 19 individual (fifth row) and a stage 24–25 individual (sixth row) of Idiosepius notoides express Pax2/5/8 in various domains. Red dashed line indicates trajectory of esophagus and internal yolk. Abbreviations: an, anus; at, apical tuft, ey, eye; f, foot; fn, funnel; g, gill; ib, interbasal lobe; m, mantle; ms, middle subesophageal mass; s, shell; sc, statocyst; sg, shell gland; se, supraesophageal mass; stm, stomach; ps, posterior subesophageal mass; pt, prototroch; y, yolk. Scale bars: 50 μm (except both last scale bars for I. notoides with 150 μm)

Mentions: The gastrula stage is reached between 3–5 h post fertilization (hpf) at 20 °C. During this stage Acr-Pax2/5/8 is expressed in ectodermal cells of the apical region (Fig. 4a–c). Early trochophore larvae hatch at approximately 12 hpf. They are lecithotrophic and are slightly ovoid in shape, with an apical organ and apical tuft in the episphere (Fig. 4d–h). The apical organ comprises three serotonin-like immunoreactive flask-shaped cells and faint FMRFamide-like immunoreactivity (Fig. 4d, e). Two other groups comprising four FMRFamide-like immunoreactive cells each are located in the episphere close to the prototroch (Fig. 4e). The episphere is separated from the hyposphere by two rows of trochoblasts that give rise to the prototroch. Acr-Pax2/5/8 is expressed in different domains, here referred to as “groups”, located mainly in the larval episphere (Fig. 4e–l). Several Acr-Pax2/5/8-expressing cells are located in the ectoderm of the dorsal episphere adjacent to both rows of trochoblasts (group 1 in Figs. 4e, j, k, l and 5). In addition, two other groups are located bilaterally and anterior to group 1 (group 2 in Figs. 4f, j, l and 5). Each group 2 comprises approximately four ectodermal cells that are located subepidermally and project dendrites through the epidermis (group 2 in Figs. 4f, j and 5). Two single Acr-Pax2/5/8-expressing cells are located bilaterally, immediately adjacent to the two rows of trochoblasts and more ventrally to group 2 in the episphere (group 3 in Figs. 4g, i and 5). In the center of the ventral episphere, a group of 5–10 ectodermal Acr-Pax2/5/8-expressing cells is present (group 4 in Figs. 4h, k, l and 5). The only Acr-Pax2/5/8 expression domain that is located in the hyposphere of the early trochophore is situated in the region of the nascent shell fields in the dorsal hyposphere (arrowheads in Figs. 4f, g, j, k and 5). The apical organ does not express Acr-Pax2/5/8 (red dashed circle in Fig. 4f, j, l). In further developed trochophore larvae (35 hpf), Acr-Pax2/5/8-expression is less pronounced in the episphere, while Acr-Pax2/5/8 expression in the hyposphere gains in intensity (Fig. 5; arrowheads in Fig. 6a, c). This and other Acr-Pax2/5/8-expressing cell groups are located in similar expression domains as described for earlier developmental stages (Fig. 5; cf. arrowheads in Fig. 4j, k with arrowheads in Fig. 6a, c). Acr-Pax2/5/8-expressing cells are present in the expression domains of groups 1, 2, and 4 of previous stages (c.f. Figs. 5 and 6a, c, d). Furthermore, serotonin-like immunoreactive cell somata are located in corresponding regions, such as the lateroventral ampullary cells corresponding to Acr-Pax2/5/8-expressing group 2, or the additional sensory cells that are located in the dorsal episphere that correspond to group 1 (Fig. 6b). In the expression domains of Acr-Pax2/5/8-expressing groups 3 and 4, FMRFamide-like immunoreactive cell somata are located (not shown). In further developed trochophore larvae (35 hpf), the apical organ does not exhibit Acr-Pax2/5/8 expression, however, very close to it, Acr-Pax2/5/8-expressing cells are located (Fig. 6c). In metamorphic competent trochophore larvae (65 hpf), the Acr-Pax2/5/8 expression pattern is similar to the one of earlier trochophores (35 hpf) (Figs. 5 and 6e–k). Strong Acr-Pax2/5/8 expression is present in cells of the nascent shell fields (Figs. 5 and 6e). These Acr-Pax2/5/8-expressing cells are located in the epidermis and project dendrites to the periphery (inset in Fig. 6j). In addition, Acr-Pax2/5/8-expressing cells are numerous in groups 1–4 during earlier development (Figs. 5 and 6f–j). Interestingly, all these Acr-Pax2/5/8 expression domains house FMRFamide-like-immunoreactive (usually flask-shaped) cells (Fig. 6j).Fig. 4


Ancestral role of Pax2/5/8 in molluscan brain and multimodal sensory system development.

Wollesen T, Rodríguez Monje SV, Todt C, Degnan BM, Wanninger A - BMC Evol. Biol. (2015)

Sketch drawings of Pax2/5/8 expression in Acanthochitona crinita, Nucula tumidula, and Idiosepius notoides. Dorsal (d)–ventral (v), apical (a)-abapical (aa), and anterior (ant)-posterior (p) axes indicate the orientation. Mouth is marked by asterisk in all panels. Pax2/5/8-expressing cell groups are indicated by red numbers in early trochophore larvae of Acanthochitona crinita (first row). Additional Pax2/5/8-expressing cells are located in the hyposphere of further developed larvae (second row). A pericalymma larva (third row) and a settled individual (fourth row) of Nucula tumidula express Pax2/5/8 in the mantle. Note that Pax2/5/8 is not expressed in the test cells (tc) that constitute the outermost cell layer. A stage 19 individual (fifth row) and a stage 24–25 individual (sixth row) of Idiosepius notoides express Pax2/5/8 in various domains. Red dashed line indicates trajectory of esophagus and internal yolk. Abbreviations: an, anus; at, apical tuft, ey, eye; f, foot; fn, funnel; g, gill; ib, interbasal lobe; m, mantle; ms, middle subesophageal mass; s, shell; sc, statocyst; sg, shell gland; se, supraesophageal mass; stm, stomach; ps, posterior subesophageal mass; pt, prototroch; y, yolk. Scale bars: 50 μm (except both last scale bars for I. notoides with 150 μm)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4625944&req=5

Fig5: Sketch drawings of Pax2/5/8 expression in Acanthochitona crinita, Nucula tumidula, and Idiosepius notoides. Dorsal (d)–ventral (v), apical (a)-abapical (aa), and anterior (ant)-posterior (p) axes indicate the orientation. Mouth is marked by asterisk in all panels. Pax2/5/8-expressing cell groups are indicated by red numbers in early trochophore larvae of Acanthochitona crinita (first row). Additional Pax2/5/8-expressing cells are located in the hyposphere of further developed larvae (second row). A pericalymma larva (third row) and a settled individual (fourth row) of Nucula tumidula express Pax2/5/8 in the mantle. Note that Pax2/5/8 is not expressed in the test cells (tc) that constitute the outermost cell layer. A stage 19 individual (fifth row) and a stage 24–25 individual (sixth row) of Idiosepius notoides express Pax2/5/8 in various domains. Red dashed line indicates trajectory of esophagus and internal yolk. Abbreviations: an, anus; at, apical tuft, ey, eye; f, foot; fn, funnel; g, gill; ib, interbasal lobe; m, mantle; ms, middle subesophageal mass; s, shell; sc, statocyst; sg, shell gland; se, supraesophageal mass; stm, stomach; ps, posterior subesophageal mass; pt, prototroch; y, yolk. Scale bars: 50 μm (except both last scale bars for I. notoides with 150 μm)
Mentions: The gastrula stage is reached between 3–5 h post fertilization (hpf) at 20 °C. During this stage Acr-Pax2/5/8 is expressed in ectodermal cells of the apical region (Fig. 4a–c). Early trochophore larvae hatch at approximately 12 hpf. They are lecithotrophic and are slightly ovoid in shape, with an apical organ and apical tuft in the episphere (Fig. 4d–h). The apical organ comprises three serotonin-like immunoreactive flask-shaped cells and faint FMRFamide-like immunoreactivity (Fig. 4d, e). Two other groups comprising four FMRFamide-like immunoreactive cells each are located in the episphere close to the prototroch (Fig. 4e). The episphere is separated from the hyposphere by two rows of trochoblasts that give rise to the prototroch. Acr-Pax2/5/8 is expressed in different domains, here referred to as “groups”, located mainly in the larval episphere (Fig. 4e–l). Several Acr-Pax2/5/8-expressing cells are located in the ectoderm of the dorsal episphere adjacent to both rows of trochoblasts (group 1 in Figs. 4e, j, k, l and 5). In addition, two other groups are located bilaterally and anterior to group 1 (group 2 in Figs. 4f, j, l and 5). Each group 2 comprises approximately four ectodermal cells that are located subepidermally and project dendrites through the epidermis (group 2 in Figs. 4f, j and 5). Two single Acr-Pax2/5/8-expressing cells are located bilaterally, immediately adjacent to the two rows of trochoblasts and more ventrally to group 2 in the episphere (group 3 in Figs. 4g, i and 5). In the center of the ventral episphere, a group of 5–10 ectodermal Acr-Pax2/5/8-expressing cells is present (group 4 in Figs. 4h, k, l and 5). The only Acr-Pax2/5/8 expression domain that is located in the hyposphere of the early trochophore is situated in the region of the nascent shell fields in the dorsal hyposphere (arrowheads in Figs. 4f, g, j, k and 5). The apical organ does not express Acr-Pax2/5/8 (red dashed circle in Fig. 4f, j, l). In further developed trochophore larvae (35 hpf), Acr-Pax2/5/8-expression is less pronounced in the episphere, while Acr-Pax2/5/8 expression in the hyposphere gains in intensity (Fig. 5; arrowheads in Fig. 6a, c). This and other Acr-Pax2/5/8-expressing cell groups are located in similar expression domains as described for earlier developmental stages (Fig. 5; cf. arrowheads in Fig. 4j, k with arrowheads in Fig. 6a, c). Acr-Pax2/5/8-expressing cells are present in the expression domains of groups 1, 2, and 4 of previous stages (c.f. Figs. 5 and 6a, c, d). Furthermore, serotonin-like immunoreactive cell somata are located in corresponding regions, such as the lateroventral ampullary cells corresponding to Acr-Pax2/5/8-expressing group 2, or the additional sensory cells that are located in the dorsal episphere that correspond to group 1 (Fig. 6b). In the expression domains of Acr-Pax2/5/8-expressing groups 3 and 4, FMRFamide-like immunoreactive cell somata are located (not shown). In further developed trochophore larvae (35 hpf), the apical organ does not exhibit Acr-Pax2/5/8 expression, however, very close to it, Acr-Pax2/5/8-expressing cells are located (Fig. 6c). In metamorphic competent trochophore larvae (65 hpf), the Acr-Pax2/5/8 expression pattern is similar to the one of earlier trochophores (35 hpf) (Figs. 5 and 6e–k). Strong Acr-Pax2/5/8 expression is present in cells of the nascent shell fields (Figs. 5 and 6e). These Acr-Pax2/5/8-expressing cells are located in the epidermis and project dendrites to the periphery (inset in Fig. 6j). In addition, Acr-Pax2/5/8-expressing cells are numerous in groups 1–4 during earlier development (Figs. 5 and 6f–j). Interestingly, all these Acr-Pax2/5/8 expression domains house FMRFamide-like-immunoreactive (usually flask-shaped) cells (Fig. 6j).Fig. 4

Bottom Line: Our results, along with those on Otx- and Hox-gene expression, demonstrate that the cephalopod condition is similar to that in mouse and fruit fly, with Otx being expressed in the anterior-most brain region (except for the vertical lobe) and a Pax2/5/8 expression domain separating the Otx-domain from a Hox-gene expressing posterior brain region.Thus, Pax2/5/8 appears to have been recruited independently into regionalization of non-homologous complex brains of organisms as different as squid, fruit fly, and mouse.In mollusks, Pax2/5/8 is only expressed in derivatives of the ectoderm and hence an ancestral role in molluscan ectoderm differentiation is inferred.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Zoology, Faculty of Sciences, University of Vienna, 1090, Vienna, Austria. tim.wollesen@univie.ac.at.

ABSTRACT

Background: Mollusks represent the largest lophotrochozoan phylum and exhibit highly diverse body plans. Previous studies have demonstrated that transcription factors such as Pax genes play important roles during their development. Accordingly, in ecdysozoan and vertebrate model organisms, orthologs of Pax2/5/8 are among others involved in the formation of the midbrain/hindbrain boundary, the auditory/geosensory organ systems, and the excretory system.

Methods: Pax2/5/8 expression was investigated by in situ hybridization during the development of representatives of the two major molluscan subclades, Aculifera and Conchifera.

Results: Compared to the investigated polyplacophoran and bivalve species that lack larval statocysts as geosensory organs and elaborate central nervous systems (CNS), cephalopods possess highly centralized brains and statocysts. Pax2/5/8 is expressed in regions where sensory cells develop subsequently during ontogenesis. Expression domains include esthetes and the ampullary system in polyplacophorans as well as the eyes of cephalopods. No Pax2/5/8 expression was observed in the less centralized CNS of bivalve, polyplacophoran, and gastropod embryos, thus arguing for a loss of Pax2/5/8 involvement in CNS development in these lineages. In contrast, Pax2/5/8 is expressed among others in brain lobes along the trajectory of the esophagus that divides the cephalopod brain.

Conclusions: Our results, along with those on Otx- and Hox-gene expression, demonstrate that the cephalopod condition is similar to that in mouse and fruit fly, with Otx being expressed in the anterior-most brain region (except for the vertical lobe) and a Pax2/5/8 expression domain separating the Otx-domain from a Hox-gene expressing posterior brain region. Thus, Pax2/5/8 appears to have been recruited independently into regionalization of non-homologous complex brains of organisms as different as squid, fruit fly, and mouse. In addition, Pax2/5/8 is expressed in multimodal sensory systems in mollusks such as the esthetes and the ampullary system of polyplacophorans as well as the eyes of cephalopods. Pax2/5/8-expressing cells are present in regions where the future sensory cells such as the polyplacophoran esthetes are situated and hence Pax2/5/8 expression probably predates sensory cell development during ontogeny. In mollusks, Pax2/5/8 is only expressed in derivatives of the ectoderm and hence an ancestral role in molluscan ectoderm differentiation is inferred.

No MeSH data available.


Related in: MedlinePlus